Intracellular Distribution of Manganese by the Trans-Golgi Network Transporter NRAMP2 Is Critical for Photosynthesis and Cellular Redox Homeostasis

Abstract

Plants require trace levels of manganese (Mn) for survival, as it is an essential cofactor in oxygen metabolism, especially O production via photosynthesis and the disposal of superoxide radicals. These processes occur in specialized organelles, requiring membrane-bound intracellular transporters to partition Mn between cell compartments. We identified an member of the NRAMP family of divalent metal transporters, NRAMP2, which functions in the intracellular distribution of Mn. Two knockdown alleles of showed decreased activity of photosystem II and increased oxidative stress under Mn-deficient conditions, yet total Mn content remained unchanged. At the subcellular level, these phenotypes were associated with a loss of Mn content in vacuoles and chloroplasts. NRAMP2 was able to rescue the mitochondrial yeast mutant In plants, NRAMP2 is a resident protein of the-Golgi network. NRAMP2 may act indirectly on downstream organelles by building up a cytosolic pool that is used to feed target compartments. Moreover, not only does the mutant accumulate superoxide ions, but NRAMP2 can functionally replace cytosolic superoxide dismutase in yeast, indicating that the pool of Mn displaced by NRAMP2 is required for the detoxification of reactive oxygen species.

Homologous Proteins of the Manganese Transporter PAM71 Are Localized in the Golgi Apparatus and Endoplasmic Reticulum

“…Because the root length of pml3 plants was not changed in comparison to wild-type in lower MnSO 4 concentrations, we assume that PML3 is involved in specific processes during Mn excess, perhaps loading Mn into the Golgi. It is believed that Mn stored in the Golgi can be remobilized by NRAMP2 in Mn deficient conditions [21,22]. In addition, an interesting phenotype was observed when PML3:GFP was overexpressed.…”

“…Two P-type ATPases, ER-type calcium ATPase 1 (ECA1) and ECA3 (which are localized to the endoplasmic reticulum and the Golgi membrane, respectively) are expressed in all major organs, and are involved in Mn pumping into these organelles [18][19][20]. Remobilization of Mn from the trans-Golgi compartment is mediated by NRAMP2 [21,22] which helps to build up/maintain the cytosolic Mn pool.…”

Manganese in Plants: From Acquisition to Subcellular Allocation

“…Nevertheless, nramp2 mutants showed a hypersensitivity to Mn deficiency and a reduction in Mn contents in vacuoles and chloroplasts with an accompanying reduction in PSII activity under those conditions (Alejandro et al, 2017). Surprisingly, the nramp2nramp3nramp4 triple mutant did not exhibit higher sensitivity to Mn deficiency than the single nramp2 and double nramp3nramp4 mutants (Alejandro et al, 2017). This suggests that the three transporters act in the same pathway to deliver Mn to the chloroplasts.…”

“…Moreover, Mn deficiency caused a decrease of cuticular waxes in Arabidopsis leaves (Alejandro et al, 2017).…”

“…Golgi/PVC Unaffected by +Mn - Delhaize et al, 2007;Peiter et al, 2007 ShMTP8 -Tonoplast -- Delhaize et al, 2003Delhaize et al, , 2007 Curie et al, 2000;Thomine et al, 2000;Cailliatte et al, 2010;Castaings et al, 2016 AtNRAMP2 Root (pericycle, root tip), leaf vasculature, flower, trichome TGN Up-regulated by -Mn down-regulated by -Fe - Curie et al, 2000;Alejandro et al, 2017;Gao et al, 2018 (Continued) (Henriques, 2004;Hebbern et al, 2009;Alejandro et al, 2017), as well as higher susceptibility to pathogen infections (Heckman et al, 2003;Heine et al, 2011), imbalance in plant water relations (Ohki, 1985;Hebbern et al, 2009), and decreased tolerance to low temperatures (Ihnatowicz et al, 2014;Stoltz and Wallenhammar, 2014). Mn deficiency leads to a reduced number of Mn-complexes in the PSII core, which causes the destabilization and disintegration of PSII complexes that lowers the net photosynthesis rate (Schmidt et al, 2016).…”